Recorded at the Georgia State Botanical Garden of Athens, GA on August 17th 2014. A carpenter ant (Camponotus spp.) colony nested at the base of a young beech tree (Fagus grandifolia) were tending aphids on the same tree. There is an interestic four level trophic interaction at this one spot forming a food chain. The parasitoid fly feeding on ants who feed on aphids sucking carbohydrate rich sap out of the beech tree:
Beech tree > Aphids > Ants > Parasitic fly
Ants are great resource utilizers. They can bypass aphids altogether if the plants provide the sweet nectar directly through extrafloral nectaries. Plants who become allies with ants get protected from herbivores.
Although aphids are well-guarded by worker ants, the ants themselves are vulnerable to parasitic attack. One of them is this Phorid fly (also know as coffin flies or scuttle flies) belonging to the genus Apocephalus who stages multiple attacks pretty much all day long if it discovers a group of ants. Normally when ants are foraging they are moving targets and are less prone to parasitic attack from flies. When ants tend aphids a trade off arises. Ants can get the sweet nectar from the aphids honeydew secretions in an open buffee manner but in return they become easy targets for parasitic flies. Aphids are “herded” into small patches on the stem by a group of worker ants. In this fashion ants form an abundant, aggregated and less mobile resource for the parasite. There are about 4-7 workers within the frame in this short observation all becoming easy targets. The fly targets the thorax twice at 0:18 and 1:03 time codes. The footage was shot with a camera at 4K resolution.
After the fly injects her eggs into the thorax of a worker ant, maggots develop inside and gradually crawl into the ants head as they feed on the ants tissues. Two weeks later the infected ant leaves the colony, in a “zombified” behavior. She walks into a habitat suitable for the pupation of fly larvae. The emerging fly crawls out through the mouth space of the ants head. Several phorid flies have been nicknamed “ant-decapitating” flies. But in every known case, the decapitation was incidental. In the following BBC footage a never-before-seen behavior is performed by another phorid fly species Dohrniphora longirostrata dicovered by Dr. Brian Brown of the Natural History Museum of Los Angeles County in California who has studied phorid flies for many years. In 2010 he serendipitously stumbled upon these flies while he was in the Brazilian woods, crushing ants with forceps as bait for ant-decapitating Apocephalus flies:
The video below shows a zombified carpenter ant worker waiting to meet her horrific death. She was most probably parasitized by a fungus (see the two videos explaining fungal parasitism further down). In both types of parasitism one thing is common in the final mortal stage: Victims loose muscle control and get in a state of parasite induced paralysis. Parasites can influence behavior of their hosts. Scientists hypothesize that parasite stress may even lead to reduction in Human intelligence since the brain consumes a whopping 20% of the total energy budget of our bodies.
Parasitized Carpenter Ant 2013 Sept 15 [105] #004 from Uzay Sezen on Vimeo.
Phorid flies can inflict a lot of damage on social insects and whether Pseudacteon Phorid flies could be used effectively to control invasive fire ants is a curious research question. These flies have been documented to attack honeybees in California. Flies are reported to carry the deformed wing virus and a fungal pathogen Nosema ceranae. Once a worker bee is attacked seven days later up to 13 Phorid larvae emerge and pupate. Researchers suspect the fly may be exacerbating colony collapse disorder in honeybee hives.
Ants may also be infected by a parasitic fungus which dramatically changes the behavior of tropical carpenter ants, causing them to become zombie-like. They die at clinging to the midrib vein of leaves increasing the spread of the fungal spores.
The zombie-like behavior induced in infected ants is so characteristic that even in 48 million year old fossil leaves found from Messel Pit in Germany bear the telltale signature bite marks on their midribs (see the video by American Museum of Natural History at the bottom).
Ants are not the only victims of Zombification. Caterpillars of the beet army worm moth (Spodoptera exigua) have been shown to be zombified by a baculovirus specific to this moth. The baculovirus known as Spodoptera exigua Multiple Nucleopolyhedrovirus (SeMNPV) alters the behavior of the caterpillars response to light. Right before the virus enters into its contagious stage, caterpillars are driven to climb to the top of the host plant. At this position as the dead body of the caterpillar decays infectious virus particles can spread to a wider area increasing the chance to infect other moths. Moreover birds may eat this easy prey and spread the virus over much larger area.
Uninfected moth caterpillars climb up and down their host plants and do not respond to changing light conditions. They remain low on the host plant. Eventually mature caterpillars come down to a safe spot at the base of the plant before becoming immobile pupae. On the other hand, 3 days after being infected caterpillars started to crawl up towards the plant tops in the presence of light. When infected caterpillars were kept in complete darkness they didn’t climb and died at lower heights. These observations confirmed that virus makes the caterpillars move toward light and they end up on top of their host plant to die.
There is an excellent article by Carl Zimmer for the Halloween Edition of National Geographic that covers some of the striking examples of parasites altering behavior of their hosts.
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